Muscle performance during frog jumping: influence of elasticity on muscle operating lengths

Abstract

A fundamental feature of vertebrate muscle is that maximal force can be generated only over a limited range of lengths. It has been proposed that locomotor muscles operate over this range of lengths in order to maximize force production during movement. However, locomotor behaviours like jumping may require muscles to shorten substantially in order to generate the mechanical work necessary to propel the body. Thus, the muscles that power jumping may need to shorten to lengths where force production is submaximal. Here we use direct measurements of muscle length in vivo and muscle force-length relationships in vitro to determine the operating lengths of the plantaris muscle in bullfrogs (Rana catesbeiana) during jumping. We find that the plantaris muscle operates primarily on the descending limb of the force-length curve, resting at long initial lengths (1.3 +/- 0.06 L(o)) before shortening to muscle's optimal length (1.03 +/- 0.05 L(o)). We also compare passive force-length curves from frogs with literature values for mammalian muscle, and demonstrate that frog muscles must be stretched to much longer lengths before generating passive force. The relatively compliant passive properties of frog muscles may be a critical feature of the system, because it allows muscles to operate at long lengths and improves muscles' capacity for force production during a jump.

Figure 1.

Methods for measuring plantaris lengths and activity during jumping. (a) The plantaris is highlighted in ventral view showing the substantial aponeurosis and tendon (white) associated with the muscle. The plantaris acts as the primary ankle extensor. (b) Sonomicrometry transducers were placed along superficial, proximal fascicles to measure length. Two bipolar EMG electrodes were also implanted in the same region to measure muscle activation patterns. (c,d) Jumps were recorded in two views with high-speed video at 250 frames s⁻¹.

Figure 2.

Muscle length, EMG and body velocity for a representative jump. (a) Fascicle lengths measured by sonomicrometry normalized to the muscle's optimal length (L_o). (b) Muscle activity during jumps. The two separate bursts of EMG activity shown occurred in many but not all jumps. (c) Plot of the body velocity during the jump measured from high-speed video. This plot shows that little external movement occurred during the period of initial muscle activation and shortening. The beginning of the jump as measured from external video often coincided with a slowing of fascicle shortening and reduced EMG activity.

Figure 3.

The force–length properties and operating lengths of the plantaris muscle. (a) Normalized force–length curves from plantaris muscles of four individuals. Active properties are shown in red and passive properties are shown in black. Each individual is represented by a different symbol. (b) Muscle operating lengths for the plantaris muscle during jumps. Fascicle length was measured with the same sonomicrometry transducers during both in vivo jumps and in vitro characterization of the force–length curves, allowing for the accurate determination of operating length during jumping. Each horizontal bar represents the mean (±s.d.) operating length for one individual. All muscles started at lengths corresponding to the descending limb of the active force–length curve and shortened onto or near the plateau. Note that the horizontal bars correspond only to values on the x-axis.

Figure 4.

The effect of operating length on the peak force production in a muscle. Using an in vitro protocol we show the same muscle undergoing two contractions (1 and 2) where the fascicles shorten by about 30 per cent. (a) Operating lengths for two ‘fixed-end’ contractions in the same muscle shortening against elastic structures in vitro. In both contractions the muscle shortens by about 30 per cent, but contraction (1) starts on the plateau, while contraction (2) starts on the descending limb. The classic Gordon Huxley & Julian (1966) force–length curve illustrates the hypothetical effect of length on force for maximally activated, isometric muscle. (b) Developed force versus time for two sample contractions consisting of length changes depicted in panel (a). Higher peak force is developed when the muscle starts at a longer length. This example shows that peak force production may be influenced more by a muscle's length at the end of a contraction than by its initial length.

Figure 5.

Meta-analysis of passive muscle properties. (a) Passive force–length curves are shown for 15 mammalian and 7 anuran hindlimb muscles. The data show that frog muscles can be stretched to longer muscle lengths relative to their optimal length (L_o) for a given force. (b) A comparison of the length (L₂₀) at which muscles reach passive forces that correspond to 20 per cent of maximum active isometric force. Anuran muscles can be stretched to significantly (p < 0.0001) longer lengths for the same level of force. Data included in this analysis were limited to published studies of hindlimb muscles that measured both active and passive force–length properties and could therefore be normalized to L_o. Mammalian data are from: Gareis et al. (1992), Woittiez et al. (1983), Hawkins & Bey (1997), Davis et al. (2003), Witzmann et al. (1982), Rack & Westbury (1969) and Askew & Marsh (1998). Anuran data are from: Bagni et al. (1988), Julian & Moss (1980), this study, Talbot & Morgan (1998), Edman (1979), Altringham & Bottinelli (1985) and Ter Keurs et al. (1978). See electronic supplementary material, figure for more detail.